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/lp/springer-journals/low-visual-information-processing-speed-and-attention-are-predictors-LuYB1eu1H6
- Publisher
- Springer Journals
- Copyright
- Copyright © 2011 by Mizuno et al; licensee BioMed Central Ltd.
- Subject
- Biomedicine; Neurosciences; Neurology; Behavioral Therapy; Psychiatry
- eISSN
- 1744-9081
- DOI
- 10.1186/1744-9081-7-20
- pmid
- 21672212
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- See Article on Publisher Site
Abstract
Background: Fatigue is a common complaint among elementary and junior high school students, and is known to be associated with reduced academic performance. Recently, we demonstrated that fatigue was correlated with decreased cognitive function in these students. However, no studies have identified cognitive predictors of fatigue. Therefore, we attempted to determine independent cognitive predictors of fatigue in these students. Methods: We performed a prospective cohort study. One hundred and forty-two elementary and junior high school students without fatigue participated. They completed a variety of paper-and-pencil tests, including list learning and list recall tests, kana pick-out test, semantic fluency test, figure copying test, digit span forward test, and symbol digit modalities test. The participants also completed computerized cognitive tests (tasks A to E on the modified advanced trail making test). These cognitive tests were used to evaluate motor- and information- processing speed, immediate and delayed memory function, auditory and visual attention, divided and switching attention, retrieval of learned material, and spatial construction. One year after the tests, a questionnaire about fatigue (Japanese version of the Chalder Fatigue Scale) was administered to all the participants. Results: After the follow-up period, we confirmed 40 cases of fatigue among 118 students. In multivariate logistic regression analyses adjusted for grades and gender, poorer performance on visual information-processing speed and attention tasks was associated with increased risk of fatigue. Conclusions: Reduced visual information-processing speed and poor attention are independent predictors of fatigue in elementary and junior high school students. Background When students proceed to junior high school from Fatigue refers to the feeling that people may experience elementary school, a multitude of changes occur in their after or during prolonged activity [1]. Fatigue is a com- environment, which have the potential to cause a variety mon symptom among students. Up to 8% of children of behavioral and emotional problems [4]. One example and adolescents have experienced fatigue for more than is the number of Japanese students exhibiting school one month, and nearly 2% have experienced chronic refusal, which was observed in 0.6% of 6th-graders and fatigue lasting more than six months [2]. Because fatigue 1.9% of 7th-graders in 2005 [5]. It has been reported that student fatigue also markedly increases from ele- in students is associated with a decrease in academic performance [3], the impact of fatigue on children and mentary school to junior high school [6]. Identifying adolescents requires additional attention. fatigue-related factors is thus important for preventing increased levels of fatigue during this transition period. Executive function is defined as a set of cognitive con- trol processes that permit goal-directed behavior and * Correspondence: keimizuno@riken.jp that develop dramatically between childhood and adoles- Department of Physiology, Osaka City University Graduate School of cence [7]. In studies on the development of executive Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka City, Osaka 545-8585, Japan Full list of author information is available at the end of the article © 2011 Mizuno et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Mizuno et al. Behavioral and Brain Functions 2011, 7:20 Page 2 of 7 http://www.behavioralandbrainfunctions.com/content/7/1/20 function, for example, age-related gain has been Methods reported in working memory [8,9], inhibitory control Participants [10], task switching [11], control of attention [12], adap- Participants were enrolled from the 4th, 5th, and 6th tive problem solving [13], and various other planning grades in an elementary school and from 7th, 8th, and and problem-solving tasks [14]. Recently, we demon- 9th grades in a junior high school in Hyogo Prefecture, strated the development of several cognitive functions in Japan, between November 2006 and December 2006 elementary school and junior high school students using [15]. Most of the students at the elementary school were paper-and-pencil and computerized cognitive function expected to proceed on to the junior high school. tests which are used in the present study as well [15]. Among 362 participants, 45 students with medical ill- Task performance of students on an auditory attention nesses, such as allergic disease, bronchial asthma, thyr- task (digit span forward test), visual information-proces- oid disease, nephritis, diabetes mellitus, heart disease, sing speed and attention tasks [symbol digit modalities anemia, myodystrophy, and epilepsy, were excluded test and tasks A and B on the modified advanced trail from the analyses. In addition, 17 students who did not making test (mATMT)], retrieval of learned material complete the fatigue questionnaire were also excluded. task (semantic fluency test), switching attention task Furthermore, 103 fatigued participants and 55 9th grade (task E on the mATMT), and a divided attention task junior high school students, who were to be graduated (kana pick-out test) improved from elementary to junior from the school after 1 year, were also excluded. Among high school. Thus, these cognitive functions develop the 142 participants, 118 cases (83.1%) were entered in a from childhood to adolescence. Based on these findings, 1-year prospective fatigue registry, between November these cognitive tests were advantageous in the present 2007 and December 2007, and 24 did not meet eligibil- study for evaluation of cognitive development in chil- ity requirement because of the failure to complete the dren and adolescents. fatigue questionnaire. The study protocol was approved Fatigue has been shown to be associated with by the Ethics Committee of Osaka City University, and impaired cognitive function in studies of adults all the participants and their parents gave written [16-19]. In children and adolescents, childhood chronic informed consent to participate in the study. fatigue syndrome (CCFS), characterized by profound and disabling fatigue persisting for at least 6 months Fatigue scale [20], can severely impair cognitive functions such as The severity of fatigue was measured using the Chalder learning, short-term memory, visual information-pro- Fatigue Scale [25]. The Chalder Fatigue Scale question- cessing speed and attention processing [21-23]. From naire was distributed to the students in a classroom at these data, impaired cognitive function appeared to be their school before the cognitive tests. The reliability associated with fatigue; however, these findings were and validity of the Japanese version of the Chalder Fati- limited to a specific disease. Therefore, we recently gue Scale for evaluation of the severity of fatigue in stu- demonstrated that fatigue was also correlated with dentswerepreviouslyconfirmed [26]. The fatigue scale reduced cognitive function in elementary and junior consists of 11 questions using a 2-level (0-1) general high school students. Slow visual motor processing was health questionnaire scale in which responses can be 0 positively correlated with the prevalence of fatigue in (less than usual or no more than usual) or 1 (more than the elementary school students and decreased visual usual or much more than usual) during the past several information-processing speed and attention processing weeks. The total score for the 11-item fatigue scale were positively correlated with the prevalence of fati- ranges from 0 to 11, with higher scores indicating a gue in junior high school students [24]. Although a greater degree of fatigue. Fatigue was defined as a score relationship between fatigue and cognitive function has of equal to or more than 4 on the Chalder Fatigue Scale been established, no studies to date have identified [25]. cognitive predictors of fatigue in these students. The ability to identify these predictors might help educa- Cognitive function tests tion professionals to develop screening procedures to Students performed a variety of paper-and-pencil and identify those at high risk for fatigue, and to conduct computerized cognitive tests [15,27]. Participants were early interventions to achieve lower incidences of and given an explanation of the rules for each cognitive test, higher rates of recovery from fatigue. Therefore, in the and before the participants performed each cognitive present prospective cohort study, we examined test, they practiced for 1 min. Half of the participants whether some low cognitive functions were indepen- performed the paper-and-pencil cognitive tests in the dently associated with the risk of fatigue in elementary classroom for around 35 min. After the paper-and-pen- and junior high school students. cil cognitive tests, participants moved to a computer Mizuno et al. Behavioral and Brain Functions 2011, 7:20 Page 3 of 7 http://www.behavioralandbrainfunctions.com/content/7/1/20 room and performed the computerized cognitive tests The cognitive demand of the symbol digit modalities within 10 min. The other half of the participants first test primarily includes visual information-processing performed the computerized cognitive tests in the com- speed and attention. The test consists of 1) a key with puter room, and then moved to the classroom and per- two rows, with nine stimulus symbols in the upper row, formed the paper-and-pencil cognitive tests. and matched numbers (1 - 9) in the lower row, and 2) a The paper-and-pencil cognitive tests consisted of a list two-row grid with the same nine stimulus symbols in the upper row and 84 blank cells for numeric responses learning test [28], kana pick-out test [23], semantic flu- inthelower row. Thefullscoreforthistestis84. The ency test [29], figure copying test [28], digit span for- time limit for performance of this test is set at 1 min ward test [30], symbol digit modalities test [31], and list recall test [28], performed in this order. and 30 s. The list learning test was used to assess immediate The list recall test was used to assess delayed memory. memory. This test consists of immediate recall of a 10- This test involves free recall of the words from the list item list of words over four learning trials. The words learning test. The list recall test was performed 30 min are semantically unrelated, characterized by early age of after the list learning test. The full score for this test is 10. acquisition and relatively high-level imagery, and were The computerized cognitive test consisted of the as phonetically unique as possible. The full score for mATMTand separate tasksA,B,C,D,and E[32,33]. this test is 40. For the mATMT, participants performed visual search The kana pick-out test requires parallel processing of trials. In this test, circles numbered from 1 to 25 are reading and picking out of letters, and also requires randomly located on the screen of a personal computer, appropriate allocation of attentional resources to the and participants are required to use a computer mouse two activities. Participants are shown a short story writ- to click on these circles in sequence, starting with circle teninJapanese kana characters. They are required to number 1. In task A, when the participant clicks on a find as many vowel symbols as possible within 2 min, target circle, the positions of the other circles also while understanding the meaning of the story. Two min remain the same. In task B, when the participant clicks after the start of the test, they are asked 10 questions on the first target circle, a new circle number 26 appears about the contents of the story over a 2 min period. on the screen. The positions of the other circles remain The Japanese kana characters consist of 66 phonetic the same. Thus, tasks A and B primarily require visual symbols that include five vowels; the story consists of information-processing speed and attention. The proce- dure for task C is the same as that for task B, except 406 symbols with 61 vowels. The kana pick-out score is that the positions of the other circles randomly change calculated as the number of kana characters picked out minus the number of kana characters missed. The full after each click on a target circle. Thus, task C primarily kana pick-out score for this test is 61, with a full com- requires visual search rather than visual information- prehension score of 10. processing speed and attention. In task D, circles num- The semantic fluency test was used to assess retrieval bered from 1 to 25 are regularly and sequentially located of learned material. This test consists of the total num- on a computer screen. Thus, task D requires no visual ber of exemplars generated for a given semantic cate- search, and only visual motor processing. In task E, cir- gory (vegetables) within 1 min. The semantic categories cles numbered from 1 to 13 and 12 kana letters (Japa- were chosen in an attempt to minimize retrieval nese phonograms) are randomly located on the screen, demands and thereby more specifically tap semantic and participants are required to use a computer mouse stores rather than retrieval strategies. to alternately click on numbers and kana; this task thus The figure copying test was used to assess spatial requires switching attention. Participants performed construction ability. This test consists of copying of a tasks A, B, C, D, and E in this order, and time limits for geometric figure comprised of 10 parts. Each part performance of the mATMT were set at 10 min. Partici- receives a 2-point score (accuracy and placement), for pants were instructed to perform the tasks as quickly atotal of20possiblepoints, andthus apossiblefull and accurately as possible. In order to assess visual scoreof 20. Thetimelimit forperformance of the test information-processing speed and attention, visual is set at 4 min. search, and attention switching, excluding effects of The digit span forward test was used primarily to visual motor processing, we calculated differences in assess auditory attention. An experimenter read a series reaction time as total reaction times on task A, B, C, or E subtracted by that on task D in the mATMT [15]. of digits at the rate of approximately one number per second and asked the participants to write on paper the digits exactly as read. The series ranged from 4 to 8 Statistical analyses digits in length and were presented in order of increas- The presented values are shown as the mean ± standard ing numbers of digits. The full score for this test is 8. deviation (SD) unless otherwise stated. We used Mizuno et al. Behavioral and Brain Functions 2011, 7:20 Page 4 of 7 http://www.behavioralandbrainfunctions.com/content/7/1/20 univariate and multivariate logistic regression analyses to Table 2 Baseline characteristics of study participants (n = 118) estimate the odds ratio (OR) per 1 SD increase of each cognitive test score for the incidence of fatigue in rela- Age (years) 11.3 ± 1.3 tion to baseline cognitive variables in the elementary Female (%) 63 (53.4) and junior high school students. We calculated the 95% Chalder fatigue scale (score) 1.5 ± 1.2 confidence interval (CI) for each OR and all p values List learning test (score) 31.9 ± 3.6 were two-tailed. A p valuelessthan.05 wasconsidered List recall test (score) 8.6 ± 1.4 statistically significant. Statistical analyses were per- Digit span forward test (score) 5.9 ± 1.1 formed using the SPSS 17.0 software package (SPSS, Symbol digit modalities test (score) 49.2 ± 13.2 Chicago, IL). Semantic fluency test (score) 9.8 ± 2.6 Figure copying test (score) 17.3 ± 2.8 Kana pick-out test Results Kana pick-out number 30.9 ± 9.8 Baseline characteristics of the study students are sum- Kana omission number 7.6 ± 6.9 marizedinTables1and2.The 118elementaryand Kana pick-out score 23.3 ± 11.8 junior high school students were not fatigued (fatigue Score for story comprehension 4.0 ± 2.0 score, 1.5 ± 1.2), because fatigued students who had the Modified advanced trail making test score of equal to or more than 4 on the Chalder Fatigue RT on task A (s) 42.6 ± 13.3 Scale [25], had been excluded from the analysis. Among RT on task B (s) 62.6 ± 18.0 the eligible 118 elementary and junior high school stu- RT on task C (s) 87.1 ± 24.3 dents followed for 1 year, 40 (33.9%) developed fatigue RT on task D (s) 14.2 ± 4.2 (fatigues score, 5.9 ± 1.4) and 78 (66.1%) did not RT on task E (s) 72.9 ± 32.4 develop fatigue (fatigue score, 1.1 ± 1.1). RT on task A-D (s) 28.4 ± 12.0 In order to identify cognitive predictors associated RT on task B-D (s) 48.4 ± 16.4 with fatigue in the elementary and junior high school RT on task C-D (s) 72.9 ± 22.7 students, univariate and multivariate logistic regression RT on task E-D (s) 58.7 ± 30.4 analyses were performed (Table 3). Although, in univari- ate logistic regression analyses, no cognitive tests RT, reaction time. Values are presented as the mean ± SD or number (%). reached statistical significance, in multivariate logistic regression analyses adjusted for grades and gender, school students [OR: 1.62, 95% CI: 1.08 to 2.43 (per 1 lower scores on the symbol digit modalities test [OR: SD increase); p = .019; Table 3]. No other scores of cog- 1.85, 95% CI: 3.03 to 1.12 (per 1 SD decrease), p = .016] nitive tests were predictors of fatigue in these students. and longer reaction time on task A of mATMT [OR: 1.88, 95% CI: 1.20 to 2.94 (per 1 SD increase), p =.006] Discussion were associated with a higher risk of fatigue in the ele- These prospective data demonstrate that lower scores mentary and junior high school students. In addition, on the symbol digit modalities test and longer reaction longer reaction times on task Bshowedatrendtoward times on tasks A and B of the mATMT were associated increasing risk of fatigue in these students [OR: 1.66, with the risk of fatigue in elementary and junior high 95% CI: 0.97 to 2.85 (per 1 SD increase), p = .065]. No school students. These findings were independent of other scores of cognitive tests were predictors of fatigue grade and gender. To our knowledge, this prospective in these students. cohort study provides the first evidence identifying cog- In task A of mATMT, even after the subtraction of nitive risk factors of fatigue in students. the reaction time associated with motor processing Tasks A and B of the mATMT primarily require (reaction time on task D), multivariate logistic regres- visual information-processing speed and attention. In sion analyses showed that longer reaction time was a contrast, task C requires visual search rather than visual predictor of fatigue in the elementary and junior high information-processing speed and attention. Although Table 1 Baseline characteristics of the five grades analyzed Elementary school Junior high school Grade level 4th grade 5th grade 6th grade 7th grade 8th grade Age range (9 - 10 years) (10 - 11 years) (11 - 12 years) (12 - 13 years) (13 - 14 years) Age (years) 9.7 ± 0.5 10.7 ± 0.5 11.7 ± 0.5 12.6 ± 0.5 13.4 ± 0.5 Female/Male 16/16 15/10 16/10 16/9 0/10 Values are presented as the mean ± SD or number. Mizuno et al. Behavioral and Brain Functions 2011, 7:20 Page 5 of 7 http://www.behavioralandbrainfunctions.com/content/7/1/20 Table 3 Univariate and multivariate logistic regression longer reaction times on tasks A and B were associated analyses of the occurrence of fatigue in elementary and with increased risk of fatigue, longer reaction times on junior high school students task C were not associated with increased risk of fatigue OR (95% CI) in the elementary and junior high school students. In Crude Multiple- addition, a lower score on the symbol digit modalities Adjusted* test, which was also used to assess visual information- Grade processing speed and attention, was associated with 4th grade Reference increased risk of fatigue in these students. These results (1.00) suggest that low visual information-processing speed 5th grade 1.22 and attention are predictors of fatigue in children and (0.37 - 3.96) adolescents. 6th grade 1.39 Fatigue is defined as the difficulty in initiating or sus- (0.44 - 4.40) taining voluntary activities [34], suggesting that abilities 7th grade 2.08 (0.67 - 6.44) or capacities for initiating and sustaining cognitive pro- 8th grade 7.29 cessing are important to maintain an unwearied condi- (1.52 - 35.03) tion. In the present study, the multiple logistic p for trend 0.005 regression analyses revealed that poor performance on Male 1.19 visual information-processing speed and attention tasks (0.56 - 2.56) were predictors of fatigue in elementary and junior high List learning test 0.93 0.82 (0.54 - 1.22) school students. These results suggest that well-devel- (0.63 - 1.37) oped abilities of visual information-processing speed and List recall test 0.91 0.79 (0.54 - 1.15) (0.64 - 1.29) attention are beneficial to prevent the development of Digit span forward test 1.06 0.87 (0.56 - 1.36) fatigue in these students. Since these cognitive perfor- (0.72 - 1.55) mances improve from elementary to junior high school Symbol digit modalities test 0.81 0.54 (0.33 - 0.89) [15], our findings in the present study might help educa- (0.55 - 1.20) tion professionals to develop screening procedures to Semantic fluency test 0.87 0.70 (0.43 - 1.13) identify not only cognitive developmental milestones but (0.58 - 1.37) also cognitive functions at high risk for fatigue, and to Figure copying test 0.89 0.77 (0.53 - 1.13) (0.62 - 1.27) conduct early interventions to achieve lower incidences Kana pick-out test of and higher rates of recovery from fatigue. Kana pick-out number 1.00 0.64 (0.37 - 1.10) We did not identify a mechanism by which low visual (0.67 - 1.50) information-processing speed and attention increased Kana omission number 0.91 0.87 (0.56 - 1.35) the risk of fatigue. In patients with CFS [26], the rela- (0.61 - 1.37) tionship between fatigue and deficits of visual informa- Kana pick-out score 1.06 0.81 (0.50 - 1.32) tion-processing speed and attention in accordance with (0.70 - 1.61) symbol digit modalities test [35-37] and task A on TMT Score for story comprehension 0.89 0.87 (0.57 - 1.32) (0.61 - 1.30) [37,38] have been shown. In a functional magnetic reso- Modified advanced trail making test nance imaging study, the lateral prefrontal and parietal RT on task A (per 1 SD 1.38 1.88 (1.20 - 2.94) cortices were activated during both tasks A and B on increase) (0.97 - 1.98) TMT [39]. Patients with CFS showed greater activation RT on task B (per 1 SD 1.21 1.66 (0.97 - 2.85) in the frontal cortex than healthy participants during a increase) (0.79 - 1.85) relatively easy task. In contrast, during a more challen- RT on task C (per 1 SD 0.99 1.21 (0.75 - 1.95) ging task, patients with CFS demonstrated reduced acti- increase) (0.65 - 1.51) vations in the lateral prefrontal and parietal cortices RT on task E (per 1 SD 1.03 1.26 (0.88 - 1.81) increase) (0.75 - 1.43) [40]. In addition, there is reduced gray-matter volume in RT on task A-D (per 1 SD 1.29 1.62 (1.08 - 2.43) the lateral prefrontal cortex in patients with CFS increase) (0.91 - 1.81) [41,42], indicating that the neural pathophysiology of RT on task B-D (per 1 SD 1.13 1.44 (0.86 - 2.42) CFS may be associated with more demanding cognitive increase) (0.74 - 1.72) processing [40]. The development of cognitive functions RT on task C-D (per 1 SD 0.72 1.10 (0.68 - 1.77) is observed in association with structural changes in the increase) (0.60 - 1.43) brain. Morphological analyses in children and adoles- RT on task E-D (per 1 SD 1.00 1.20 (0.84 - 1.72) increase) (0.72 - 1.38) cents have shown that brain maturation occurs at differ- ent rates in different brain regions: the primary sensory *Adjusted for grade and gender. RT, reaction time; OR, odds ratio; CI, confidence interval. and motor areas are the first to complete development, Mizuno et al. Behavioral and Brain Functions 2011, 7:20 Page 6 of 7 http://www.behavioralandbrainfunctions.com/content/7/1/20 Science, 6-7-3 Minatojima-minamimachi, Chuo-ku, Kobe City, Hyogo 650- while the association areas, especially in the frontal and 0047, Japan. Department of Medical Science on Fatigue, Osaka City parietal regions, are the last to mature [43]. Maturation University Graduate School of Medicine, 1-4-3 Asahimachi, Abeno-ku, Osaka of the frontal and parietal regions is of great importance City, Osaka 545-8585, Japan. Department of Clinical, Health and Special Needs Education Needs, Hyogo University of Teacher Education, Graduate for adequate processing of developed cognitive functions School of Education, 942-1 Shimokume, Kato City, Hyogo 673-1494, Japan. which require activation of these brain regions. In fact, task performance on visual information-processing Authors’ contributions KM took part in the planning and designing of the experiment and speed and attention improves from elementary to junior cognitive tests, data analyses and manuscript preparation. MT contributed to high school [15]. Although findings of patients with CFS the design and planning of the experiment and cognitive tests, data by neuroimaging and morphometry studies were limited analyses and manuscript preparation. SF, EY and YS contributed to the design and planning of the experiment and in data preparation. KIM to a specific adult disease, and further studies are neces- contributed to the design and planning of the experiment and recruited the sary to determine whether these findings can be general- participants. YW took part in the planning and design of the experiment ized to healthy elementary and junior high school and cognitive tests and helped write the manuscript. All authors read and approved the final manuscript. students, impaired development of frontal and parietal brain regions might introduce fatigue in the elementary Competing interests and junior high school students. The authors declare that they have no competing interests. Received: 22 February 2011 Accepted: 14 June 2011 Limitations Published: 14 June 2011 The present study has two limitations. First, we performed this study with a limited number of participants. To gener- References 1. Boksem MA, Tops M: Mental fatigue: costs and benefits. 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Behavioral and Brain Functions – Springer Journals
Published: Jun 14, 2011